Responses to social and environmental stress are attenuated by strong male bonds in wild macaques

aPrimate Social Evolution Group, Courant Research Centre Evolution of Social Behaviour, Georg-August University, Göttingen 37077, Germany;bApplied Behavioural Ecology and Ecosystems Research Unit, University of South Africa, Florida 1710, South Africa;

Significance

Male macaques form social bonds similar to human friendships that buffer them against day-to-day stressors. If male primates live in multimale groups they usually fight fiercely over access to females, but males can develop friendly relationships with a few group mates. The strength of these “friendships” has now been shown to buffer against the negative effects of social and environmental stressors, a phenomenon that was previously only described for females and pair-living animals. Long-term glucocorticoid (stress hormone) elevation can increase susceptibility to disease and mortality. This study shows that variation in everyday stressors such as the amount of aggression received or cold stress can cause such long-term elevated glucocorticoid levels but that keeping a few close male associates will avoid that.

Abstract

In humans and obligatory social animals, individuals with weak social ties experience negative health and fitness consequences. The social buffering hypothesis conceptualizes one possible mediating mechanism: During stressful situations the presence of close social partners buffers against the adverse effects of increased physiological stress levels. We tested this hypothesis using data on social (rate of aggression received) and environmental (low temperatures) stressors in wild male Barbary macaques (Macaca sylvanus) in Morocco. These males form strong, enduring, and equitable affiliative relationships similar to human friendships. We tested the effect of the strength of a male’s top three social bonds on his fecal glucocorticoid metabolite (fGCM) levels as a function of the stressors’ intensity. The attenuating effect of stronger social bonds on physiological stress increased both with increasing rates of aggression received and with decreasing minimum daily temperature. Ruling out thermoregulatory and immediate effects of social interactions on fGCM levels, our results indicate that male Barbary macaques employ a tend-and-befriend coping strategy in the face of increased environmental as well as social day-to-day stressors. This evidence of a stress-ameliorating effect of social bonding among males under natural conditions and beyond the mother–offspring, kin or pair bond broadens the generality of the social buffering hypothesis.

Strong affiliative social relationships exert powerful beneficial effects on an individual’s health and fitness in both humans and nonhuman animals (1⇓⇓⇓–5). One well-studied mediating mechanism, conceptualized in the social buffering hypothesis, is that the presence of a close social partner attenuates the reactivity of the hypothalamic–pituitary–adrenal (HPA) axis (apart from other positive effects on physiological responses) and thus buffers against the potentially adverse effects of physiological stress (4, 6, 7). Evidence for the social buffering hypothesis rests primarily on experimental studies exposing subjects to stressful situations when a close social partner is present or absent (6⇓–8). In that sense, previous studies on the social buffering effect captured an interaction effect of social bonding and a stressor, usually via exposure to a novel environment or, in humans, psychological stress on the stress response (4).

The individual functioning as a social buffer against stress is usually a pair-bonded partner [in humans and nonhuman animals (6, 8⇓⇓–11)] or mother [in infant nonhuman animals (11⇓–13)]. The “tend-and-befriend” stress-coping-mechanism (i.e., turning to close affiliates and kin), when under stress, has been linked to the attachment–caregiving system partly regulated by the oxytocinergic system (14⇓–16). Possibly as a direct consequence of this, humans exhibit a strong sex difference in behavioral coping mechanisms to perceived stressful events; women are more likely to seek social support in stressful situations compared with men (ref. 17, but see ref. 18). Stress alleviation via social support has also been shown in nonhuman primates where females with stronger bonds or a tighter social network showed an attenuated response to stressors compared with those with weaker social ties (19, 20). For example, the death of a close female partner (catastrophic stressor), usually kin, in baboons led to increased physiological stress, and the bereaved partner attempted to alleviate this response by strengthening existing bonds (21). After a conflict event in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) closely bonded bystanders can actively console recipients of aggression, thereby reducing behavioral measures of stress (22⇓–24). Many nonhuman primate females live in closely interwoven matrilineal networks of mutual affiliation and support (25⇓–27) that generate strong fitness advantages in terms of increased reproductive rates and survival (1, 28, 29).

Because most males compete for opportunities to fertilize females (30) the focus of studies investigating correlates of male physiological stress have historically been on reproductive competition and hierarchical status (31⇓–33). Nevertheless, recent and increasing evidence has shown that males of some vertebrate species also form strong social bonds that can enhance their fitness (refs. 34⇓⇓⇓–38 and reviewed in ref. 39). However, to date social buffering effects on acute HPA responses in adult male vertebrates have been investigated predominantly in pair-living species (or pair-housed animals) in response to the female pair partner’s presence (reviewed in ref. 6). It remains to be shown whether the human sex difference in behavioral stress-coping mechanisms is exhibited by other mammals as well or whether males, like females, experience social buffering responses under stress when they have strong social ties to other same-sex individuals in their group.

Similar to philopatric female baboons and male chimpanzees (38, 40, 41) macaque males of some species, including Barbary macaques (Macaca sylvanus), form strong social relationships with a few male partners (35, 36, 39, 42) that are stable over consecutive years and characterized by equitability in exchanges of affiliation (37). The mechanisms guiding partner selection for the formation of social bonds in male macaques are currently unknown. Parallel dispersal has been observed (43), and in large provisioned groups maternal relatedness partly drives agonistic support (44), but the strength of male social bonds is not decreased in maternally unrelated males in the wild (35). Males vary in the number and strength of social bonds they form (37), which may partly be guided by age (36, 45) and may additionally be affected by personality (46, 47).

Barbary macaque males frequently experience noncatastrophic stressful situations in their daily lives that may be social or environmental. Within-group conflicts resulting in aggression represent a social stressor that is positively correlated to glucocorticoid levels (a measure of physiological stress) across many primates (19, 48⇓⇓–51). Within-group aggressive conflicts also vary between individuals (50, 52) and between seasons, with peaks during the mating season (36). An annually recurring environmental stressor in the study population of Barbary macaques is cold stress during the winter months. Winter survival probability was found to be predicted by the number of affiliative relationships an individual formed (53). In baboons temperature stress is associated with increased glucocorticoid levels (54, 55).

Here we took advantage of this macaque system of strong male bonding and the occurrence of several stressors in an individual’s daily life to test the social buffering hypothesis in a natural situation and within the male sex. As the buffering hypothesis proposes that social support or bonding is related to well-being only during stressful situations (4), we predicted an interaction effect: As stressor intensity increases (i.e., rate of aggression received increases or minimum temperature declines), the attenuating effect of an individual's social bond strength on faecal glucocorticoid metabolite (fGCM) levels becomes stronger. We also controlled for an alternative, not mutually exclusive, hypothesis, the “immediate effects hypothesis,” stating that affiliative social behavior directly alleviates physiological stress irrespective of the social relationship the partners feature (20, 56, 57). For this, we tested the proximate effects of rates of grooming given and received by all group members, grooming with the top three male partners, or frequency of male–infant–male triadic interactions on fGCMs.

Results

Social bond strength was measured on a dyadic level via the composite sociality index (CSI) (Materials and Methods) comprising eight correlated measures of affiliative behavior. The male dyads with the highest 10% of CSI scores (n = 18) would, on average, be 12 times more likely to groom (0.12 vs. 0.00 interactions per hour) than dyads with the lowest 10% of CSI scores (n = 18); be twice as likely to sit in body contact (0.04 vs. 0.02 interactions per hour); be 20 times more likely to have male–infant–male triadic interactions (0.20 vs. 0.00 interactions per hour); and be 13 times more likely to be in social proximity (0.13 vs. 0.01 interactions per hour). To measure effects of the strength of a male’s social bonds instead of the effects of the number of affiliation partners we kept the number of partners constant and used the added CSI values of an individual’s top three relationships in our models. Stressor intensities varied widely from 0–13 bouts of aggression received per hour by an individual male and mean minimum daily temperature varied from −1 to +33 °C throughout the study across 10-d periods. Average individual fGCM levels increased with increasing stressor intensities for many individuals (Figs. S1 and S2). The rates of aggression received were variable for both males with strong and weak social bonds (the range of males’ summed top three CSI scores for the four quartile ranges of aggression received were as follows: low aggression, 0.5–11.1; low–mid aggression, 0.5–11.1; mid–high aggression, 0.5–12.9; and high aggression rate received, 0.7–12.9). Higher-ranked males did not necessarily have higher social bond strength; mean CSI score of a male’s top three social partners was not significantly correlated to a male’s mean dominance rank (Spearman’s rank correlation: rs = −0.144, df = 12, P = 0.62).

Immediate Effects Hypothesis.

We constructed a linear mixed model (LMM) (58) to examine both the immediate effects and social buffering hypotheses. We found no support for the immediate effects hypothesis because none of our independent behavioral variables (grooming given or received to all group members, grooming with the top three male partners, or frequency of male–infant–male triadic interactions) had an alleviating influence on fGCM levels (Table 1), even if models were run without the interaction terms of stressors and social bond strength (Table S1). We found that fGCM levels during the mating season (mean ± SD = 492.9 ± 207.8; range = 89.6–1,148.2 ng/g feces) were higher than during the nonmating season (mean ± SD = 344.1 ± 153.4; range = 71.5–1,043.1 ng/g feces) (Table 1; full vs. null model: χ2= 156.6, df = 13, P < 0.001, n = 437).

Results of an LMM with Gaussian error structure for the relationship between mean fGCM levels and social and environmental factors

Social Buffering Hypothesis.

We found the interaction between the number of aggressive bouts a male received and the strength of his top three social bonds to have a significant influence on fGCM levels (Table 1 and Fig. 1). At low levels of aggression, male social bond strength did not influence fGCM levels. However, as rates of aggression received increased, the weaker the social bond strength an individual had the higher his fGCM levels were, and this effect became stronger the higher the levels of aggression received. The interaction between mean minimum daily temperature (range of −1 to +33 °C) and the strength of a male’s bonds with his top three social partners also significantly influenced his fGCM levels (Table 1 and Fig. 2). Specifically, at the lowest mean minimum daily temperatures the weaker a male’s social bond strength was the higher his fGCM levels were. As mean minimum daily temperatures increased to mid–high levels the relationship between social bond strength and fGCM levels was much weaker. At highest mean minimum daily temperatures social bond strength seemed to have a very slight positive effect on fGCM levels; the stronger a male’s social bonds the marginally higher his fGCM levels were. Time spent in body contact was not a predictor of fGCM, indicating that the social bond strength–minimum temperature interaction effect on fGCMs was not a direct thermoregulatory consequence of more closely bonded males spending more time in body contact.

The interaction effect of social bond strength (CSI) and rate of aggression received on fGCM levels (log nanograms per gram of feces). CSI relates rates and durations of affiliative behaviors of a dyad to the respective group means across dyads. The x axis shows z-transformed values for the added CSI values of a male’s top three social bonds. For illustration data are split into four subsets representing the quartiles of aggression rate: (i) low, 0.0–0.7 bouts per hour (sky blue); (ii) low–mid, 0.8–2.2 bouts per hour (slate blue); (iii) mid–high, 2.3–5.8 bouts per hour (navy blue); and (iv) high, 5.8–13.1 bouts per hour (black); colors run in order of stressor intensity, with darker being higher levels of stressor. This visualization of raw data is not a substitute for the full statistical model results, which are presented in Table 1.

The interaction effect of social bond strength (CSI) and mean minimum daily temperature on fGCM levels (log nanograms per gram of feces). CSI relates rates and durations of affiliative behaviors of a dyad to the respective group means across dyads. The x axis shows z-transformed values for the added CSI values of a male’s top three social bonds. For illustration data are split into four subsets representing the quartiles of mean minimum daily temperature: (i) low, −0.9 to 7.5 °C (black); (ii) low–mid, 7.5–15.9 °C (navy blue); (iii) mid–high, 15.9–23.4 °C (slate blue); and (iv) high, 23.4–33.0 °C (sky blue); colors run in order of stressor intensity, with darker being higher levels of stressor. This visualization of raw data is not a substitute for the full statistical model results, which are presented in Table 1.

Discussion

This study tested predictions from the immediate effects and social buffering hypotheses in a nonhuman primate species characterized by strong male–male bonding by investigating the effects of different stressors on HPA axis activation. We show that the higher the rate of aggression received from group mates (social stressor) the stronger the attenuating effect of a male’s social bond strength on his fGCM levels. Male–male social bonds seem to provide a buffer against the negative effects of noncatastrophic daily stressors by reducing the physiological stress response. These social bonds can buffer against both social and environmental stressors, as emphasized by our finding that the lower the minimum mean ambient temperature, the stronger the negative effect of a male’s social bond strength on his fGCM levels became, providing further support for the social buffering hypothesis. This latter result was not explained by the beneficial effects of social thermoregulation via contact sitting that can characterize closely bonded dyads. From Fig. 2 it may be concluded that at highest minimum temperatures social bond strength had a slightly positive effect on fGCM levels. Fig. 2 shows a plot of raw data uncorrected for random and fixed effects and is only an illustration of the statistical interaction effect that should not be interpreted without consideration of model outcomes. Future investigations that specifically target the warmest months, that coincide with the birth season, may elucidate whether the relationship between social bond strength and fGCMs is reversed, possibly as a consequence of increased rates of infant handling (42), which did not affect our overall model outcome. The immediate effects hypothesis was not supported because the frequency or duration of affiliative behaviors did not have a significant direct impact on physiological stress levels.

Chronically elevated glucocorticoid levels in response to aggression received from group mates is a major cost of group living for subordinates in many mammals (19, 49⇓–51, 59). Several studies, however, failed to replicate the negative effect of aggression received on an individual’s physiological stress level (55, 60⇓⇓–63). Our results suggest that in these latter studies interaction effects in the social buffering mechanism may have blurred the patterns observed and may explain ambiguities between some studies and species. This highlights that limiting the analysis to the main effects of behavioral or environmental factors on physiological stress by examining factors independently can miss the subtle interactions between behavioral and environmental factors (64).

Primate social bonds are thought to be formed and maintained through a suite of affiliative behaviors including grooming or male–infant–male triadic interactions that individually have no effect on HPA axis activation (39, 65). This seems to suggest that the stress response of males with strong social bonds is buffered by the combined direct effects of these behaviors. It is important to realize, though, that not all grooming is equal. Peripheral urinary oxytocin levels measured after a single grooming interaction suggest that individuals react to the same behavioral interaction (i.e., a grooming event) differently depending on the identity of their interaction partner. Oxytocin levels after grooming are much higher in strongly bonded partners compared with two individuals with overall low rates and durations of affiliation (66). Thus, it is not surprising that the independent effects of the behaviors that comprise the social bond measure did not affect fGCM levels. A male’s position in the dominance hierarchy also did not influence his physiological stress levels, which may be due to the relative stability of the hierarchies in our study groups. Dominance rank was not correlated to the strength of a male’s top three social bonds.

Our study extends the current literature; we found that dispersing primate males that form strong social bonds (37), seem to turn to close same-sex companions in stressful situations, indicative of a tend-and-befriend stress-coping mechanism that was previously thought to be characteristic of females (14⇓–16). Mammalian females usually remain in their natal group (67) and their strongest social bonds are often with kin, particularly mothers and daughters, and as such females are expected to affiliate more frequently with these bonded partners under stressful situations (14⇓–16). Because this phenomenon may be mediated by the oxytocinergic system (14⇓–16) it is postulated to develop more easily in females than in males owing to the role of oxytocin in female care-giving toward, and attachment to, their own offspring in many mammalian species (14⇓–16). Mammalian males, in general, use highly competitive reproductive strategies and therefore are proposed to use a “fight or flight” response to stressful situations (68), mediated by the androgenic system (14⇓–16). Conversely, we found in our study that primate males may employ a mechanism similar to the female “tend and befriend” (69).

Previous support for the social buffering hypothesis in males usually came from pair-living species, pair-housed animals, or experiments with preferred female partners where male physiological stress responses were alleviated in the presence of their female partner (reviewed in refs. 6, 7, and 59). Here we show that in the wild, and similar to females, the social bonds that males form with same-sex group members provide them with a buffer against both naturally occurring social and environmental stressors. Although rare among mammals, strong social bonds between males can yield a number of adaptive benefits, including increased social status and mating and paternity success (34, 35, 37, 39, 70). Male macaques cooperate frequently with bonded male partners in agonistic coalitions (35, 37, 71, 72). Thus, as in humans and other mammals, individuals with strong social bonds may benefit from greater social support from other group members (4, 6, 7, 59). Conversely, individuals that form only weak social relationships may react to stressors more strongly, for example via impairing the regulatory function of the HPA axis (6, 7, 59). Dysregulation of the HPA axis increases susceptibility to disease (73, 74). Among captive rhesus macaques (Macaca mulatta) social stressors led to increased susceptibility to disease in individuals with a personality characterized by low sociability compared with individuals with high sociability (75). Together with the finding that in humans several negative health consequences and increased mortality are related to increased feelings of loneliness (76, 77), these results suggest that the effect of sociality (formation of strong bonds) on responsiveness to stressors may be mediated by temperament. This is echoed in cercopithecine females where individuals with a loner personality (low rate of social interactions) had higher physiological stress levels (fGCMs) than those exhibiting more highly social personalities while controlling for dominance rank (46). Experimental evidence for social buffering effects suggests that a perceived lack of social support causes physiological stress. It is less clear whether the established negative effects of elevated glucocorticoid levels on social memory and judgment may keep individuals from forming strong ties (78, 79). This would create a feedback loop with individuals that cannot cope well with stressors being more erratic in their social behavior and thus less able to form or maintain long-term social relationships. Our findings may motivate further research into the relationships between social behavior, glucocorticoids, and social cognition.

In humans, males and females frequently turn to close companions in times of high stress (14), and this is usually a core of three to five individuals (80, 81). Philopatric female nonhuman primates that lack these few strong bonds show increased mortality and reduced offspring survival (1, 28, 29), whereas those who established and maintained strong bonds to a few partners coped better with stressful situations (19⇓–21) and lived a longer life. Our results contribute to these findings by showing that wild, nonphilopatric males also benefit from maintaining strong bonds to their top partners via attenuated responses to noncatastrophic daily stressful situations. Therefore, our study suggests that the ways in which social mammals affiliate, cooperate, and compete among each other is not fundamentally different in gregarious males and females (35, 39, 66, 82, 83). Thus, the attenuation of the stress response triggered by diverse sources is yet another adaptive benefit accruing from the establishment and maintenance of strong social bonds in either sex.

Materials and Methods

Subjects and Behavioral Observations.

Data were collected from two wild groups [“green” (Gn) and “scarlet” (Sc)] of Barbary macaques living in a deciduous cedar and oak forest in the Middle-Atlas Mountains of Morocco (84). The groups consisted of seven to nine adult males and eight adult females (Gn) and six males and eight females (Sc). Data were collected on the Gn group from October 2009– April 2011 and on the Sc group from July 2010–April 2011. This study adhered to the legal requirements of Morocco, Germany, and Great Britain.

Data of all social and agonistic behaviors were collected through 40-min focal sampling (85) of all males, giving a total of 2,033 h (1,676 h Gn and 358 h Sc) of behavioral data (Supporting Information, section 1). At the beginning of each focal follow, we recorded air temperature using a 3500 Kestrel Pocket Weather Station by placing the weather station in the shade at 1.5 m above the ground (84). Social behaviors recorded included grooming, infant carrying, male–infant–male triadic interactions (37), and time spent in body contact with other group members. Social relationship quality was measured using the CSI (1) built from eight correlated affiliative behaviors: both the duration and number of interactions of grooming, body contact, male–infant–male triadic interactions, and time spent in social proximity of <1.5 m) calculated for 4-mo periods during the study (ref. 37 and Supporting Information, section 2). Following Silk et al. (1) and Schülke et al. (35), who described adaptive benefits of strong social bonds, we used the combined top three social bond values per male (i.e., the sum of his three highest CSI scores) to determine the strength of his social bonds for each 4-mo period. Thus, the effects we describe concern the strength of a male’s bonds, not their number. Dominance hierarchies where constructed from decided dyadic agonistic conflicts separately for each group using corrected normalized David’s scores (86) (Supporting Information, section 3).

Fecal Sample Collection and Analysis.

Fecal samples were collected from males between 0700 and 1900. We collected approximately one sample per male per week throughout the study period (mean ± SD: Gn, 66.63 ± 8.78; Sc, 24.00 ± 7.04 samples per male). A total of 533 (Gn) and 144 (Sc) samples were collected and transferred in a frozen state to the endocrinology laboratory at the German Primate Centre for analysis of fGCMs using previously established methods (refs. 87⇓–89 and Supporting Information, section 4).

Statistical Analysis.

To investigate both the immediate effects and social buffering hypotheses and the influence of several social factors on fGCM levels we adopted the following approach. Aggressive behaviors are sporadic in nature. Thus, to ensure accurate measurements and assuming medium-term stability of aggression rates, we calculated aggression rates from focal data collected for one male over the course of 10 d. Ten days were considered as the shortest period over which an accurate measure of aggression rate could be generated with the protocol we used. The occurrence of counteraggression can affect behavioral stress responses in primates (90), so we based our analyses solely on proactive aggression received in conflicts without counteraggression (only 2.5% of aggressive interactions involved counteraggression). This aggression rate value was then matched to the average fGCM value obtained from the one to three fecal samples collected in the corresponding 10-d period (allowing for a 2-d lag in hormone excretion). We used 2 d because changes in blood hormone levels can be detected in fecal hormone metabolite levels after about 24–56 h in macaques in radiometabolism studies and experimentally induced HPA axis activation experiments (87, 91). We then constructed an LMM (58) to examine the effect of the social factors on fGCM levels. fGCM values constituted the dependent variable and were log-transformed to achieve a symmetric distribution (n = 437).

The following behavioral and environmental measures were calculated for each of the 10 d periods, as done with the rates of aggression received above, and included as predictor variables: (i) total time spent giving grooming to all noninfant group members (seconds per focal hour), (ii) total time spent receiving grooming from all noninfant group members (seconds per focal hour), (iii) number of aggressive interactions received (per focal hour), (iv) ordinal rank position, (v) sum of top three CSI scores, (vi) total time spent carrying an infant (seconds per focal hour), (vii) number of male–infant–male triadic interactions (per focal hour), (viii) total time spent grooming with the top three social partners (seconds per focal hour), (ix) time spent in body contact with all noninfant group members (seconds per focal hour), and (x) mean minimum daily temperature. We also included season (categorical: mating or nonmating season) as a control variable. When temperatures are low, individuals may attempt to sit in body contact to maintain thermoregulation (53); thus, to control for this effect we included time spent in body contact with adult and juvenile group members as a predictor variable. To investigate the social buffering hypothesis we included two interaction terms in the model between (i) the number of aggressive bouts received and the sum of the top three CSI scores and (ii) the mean minimum daily temperature and the sum of the top three CSI scores. Note that in models with significant interaction terms the main effects of the interacting predictors cannot be interpreted reliably (92). All predictor variables were z-transformed. Group and male identity were included as random factors. We fitted the LMM with Gaussian error structure and ran the model in R version 2.15.0 (93). All assumptions of the model were respected. Collinearity between predictor variables was not a problem as all variance inflation factors were below 2 (94) (Supporting Information, section 5). Where appropriate, we report mean values ± SD. The level of significance was set at α < 0.05.

Acknowledgments

We thank Professor Mohamed Qarro (Ecole Nationale Forestière d’Ingénieurs, Morocco) for his support in the field and the Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification of Morocco for research permission; Michael Madole, Dave Thomas, Sofia Santos, Maria Thunström, Tom Smith, Josephine Msindai, and Sabine Hähndel for assistance with fieldwork; Andrea Heistermann and Petra Kiesel for providing assistance and expertise during hormone analysis; Christof Neumann for statistical advice; Laëtitia Maréchal, Rebecca Rimbach, and Cédric Girard-Buttoz for helpful comments and discussions on earlier omnishambles of this manuscript; and the editor and two anonymous reviewers for insightful comments on the manuscript. Financial support was provided by the Max Planck Society, the Christian Vogel Fond, and Georg-August University through funds from the German Initiative of Excellence.

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